Functional genes as markers for sulfur cycling and CO2 fixation in microbial communities of hydrothermal vents of the Logatchev field

Abstract

Life at deep-sea hydrothermal vents depends on chemolithoautotrophic microorganisms as primary producers mediating the transfer of energy from hydrothermal fluids to higher trophic levels. A comprehensive molecular survey was performed with microbial communities in a mussel patch at the Irina II site of the Logatchev hydrothermal field by combining the analysis of 16S rRNA gene sequences with studies of functional key genes involved in biochemical pathways of sulfur oxidation-reduction (soxB, aprA) and autotrophic carbon fixation (aclB, cbbM, cbbL). Most significantly, major groups of chemoautotrophic sulfur oxidizers in the diffuse fluids differed in their biosynthetic pathways of both carbon fixation and sulfur oxidation. One important component of the community, the Epsilonproteobacteria, has the potential to grow chemoautotrophically by means of the reductive tricarboxylic acid cycle and to gain energy through the oxidation of reduced sulfur compounds using the Sox pathway. The majority of soxB and all retrieved aclB gene sequences were assigned to this group. Another important group in this habitat, the Gammaproteobacteria, may use the adenosine 5'-phosphosulfate pathway and the Calvin-Benson-Bassham cycle, deduced from the presence of aprA and cbbM genes. Hence, two important groups of primary producers at the investigated site might use different pathways for sulfur oxidation and carbon fixation.

Ecological succession leads to chemosynthesis in mats colonizing wood in sea water

“…However, the ATP citrate marker gene (ACLY), the key enzyme of the rTCA cycle, was not found in the beginning of the colonization indicating the microbial community incapacity to run the rTCA cycle during the first development stage. The rTCA pathway is widely used by Epsilonproteobacteria (Campbell and Cary, 2004;Hügler et al, 2010) to fix carbon dioxide in anaerobic or microanaerobic conditions, which confirms that our community has acquired the potential to fix inorganic carbon between 32 and 45 days of immersion. The fact that we observed a decrease of the number of sequences related to the Bacteroidetes starch sequestration system further corroborates the hypothesis that the upper layer of the microbial mat became less dependent on the wood carbon with time.…”

Single Cells within the Puerto Rico Trench Suggest Hadal Adaptation of Microbial Lineages

“…One of the amphipod-associated cells, PRT Marinosulfonomonas, clustered within a major clade of primarily uncultivated environmental samples isolated from deep trenches, hydrothermal vent plumes, and Riftia tube worms (42). PRT Marinosulfonomonas is closely related to the alphaproteobacterium Rhodobacterales strain PRT1, a piezophilic microorganism cultured from the PRT ( Fig.…”

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

“…That the presence of an electron donor increases the carbon fixation rate indicates that Na 2 S 2 O 3 , and Fe 2 þ at least contribute to fuelling R. exoculata epibionts, and our autoradiography data suggest that chemosynthesis occurs at least in the large filamentous bacteria (epsilonproteobacteria of Marine Group 1), which appeared more intensely labelled than the thin filamentous and rod-shaped ones (epsilonproteobacteria of Marine Group 2 and gammaproteobacteria). The view that R. exoculata epibionts have sulphide-oxidising activity is consistent, moreover, with the fact epsilon-and gammaproteobacteria are assumed to have such activity, on the basis of the group affiliation of the former (Petersen et al, 2009;Goffredi, 2010;Guri et al, 2012) and because the latter possess functional SoxB and aprA genes (Hü gler et al, 2010(Hü gler et al, , 2011. We cannot say, however, what the epibiotic bacteria of R. exoculata use as predominant energy source.…”

“…By combining 16S rRNA and functional gene analysis with in-situ hybridisation and transmission electron microscopy observations on R. exoculata epibionts and their free-living or symbiotic relatives from vent habitats, investigators (Campbell et al, 2006;Zbinden et al, 2008;Petersen et al, 2009;Goffredi, 2010;Hü gler et al, 2010Hü gler et al, , 2011Guri et al, 2012) have evidenced epsilonproteobacteria of Marine Groups 1 (the new family Thiovulgaceae) and 2, as thick (3-mm wide) and thin (1-mm wide) filaments, respectively. Both should oxidise sulphur compounds through the Sox pathway and fix carbon through the reverse tricarboxylic acid cycle (SoxB and aclA gene sequences).…”

“…Authors have also identified gamma-proteobacterial epibionts of the Thiotrichaceae family (Leucothrix group), together with some free-living members and some other invertebrate ectosymbionts, mainly of crustaceans (Goffredi, 2010). These gammaproteobacteria appearing at least as filamentous and rod-shaped morphotypes can probably grow as sulphide oxidisers, most likely using the APS pathway for energy generation and the Calvin-Benson-Bassham cycle for carbon fixation (aprA and cbbM gene sequences, respectively) (Zbinden et al, 2008;Hü gler et al, 2010Hü gler et al, , 2011Guri et al, 2012). In addition, coccoidshaped cells with intracytoplasmic membrane stacks have been identified as type-I methanotrophic gammaproteobacteria (pmoA gene sequence) (Corbari et al, 2008a;Zbinden et al, 2008;Guri et al, 2012), and deltaproteobacteria related to Desulfocapsa have been identified thanks to their aprA and hydrogenase gene sequences (Hü gler et al, 2011), suggesting they can grow lithotrophically using hydrogen as electron donor for sulphate reduction.…”